Surg Radiol Anat DOI 10.1007/s00276-014-1272-z

Anatomic Variations

Variant middle meningeal artery origin from the ophthalmic artery: a case report David Kimball · Heather Kimball · R. Shane Tubbs · Marios Loukas 

Received: 14 October 2013 / Accepted: 13 February 2014 © Springer-Verlag France 2014

Abstract  We present a rare case of a variant middle meningeal artery (MMA) originating from the ophthalmic artery. During cadaveric dissection of the cranial base of an adult female, it was noted that the foramen spinosum was absent unilaterally. After identifying the MMA, its origin was traced back to the ophthalmic artery within the orbit. Although exceedingly rare, a variant MMA originating from the ophthalmic artery should be kept in mind by surgeons during skull base procedures in order to avoid unwanted complications including potential retrograde thrombosis of the ophthalmic artery with MMA manipulation or coagulation. Keywords  Anatomy · Middle meningeal artery · Variation · Foramen spinosum

within the infratemporal fossa. After entering the middle cranial fossa through the foramen spinosum, it bifurcates into anterior and posterior branches [5, 9, 10]. There is a common, but often overlooked, anastomosis that exists between the anterior branch of the MMA and the lacrimal artery (Fig. 1a) in up to 96 % of adults [10]. This anastomotic ramus of the MMA joins the lacrimal artery, a branch of the ophthalmic artery, through either the meningo-orbital foramen or superior orbital fissure [2, 4, 12]. The branch that runs through the superior orbital fissure is referred to as the sphenoidal artery, while the branch that runs through the meningo-orbital foramen is referred to as the meningolacrimal artery [2]. An MMA arising directly from the sphenoidal artery (Fig.  1b) is a very rare arterial variation [1, 4, 6, 10, 12]. This report provides a gross anatomic photographic display of a case of MMA arising from the ophthalmic artery.

Introduction The middle meningeal artery (MMA) normally arises from the mandibular portion of the internal maxillary artery between the lateral pterygoid muscle and sphenomandibular ligament [5, 10]. It ascends to the base of the skull and passes between the two roots of the auriculotemporal nerve D. Kimball · H. Kimball · M. Loukas (*)  Department of Anatomical Sciences, School of Medicine, St. George’s University, Grenada, West Indies e-mail: [email protected] R. Shane Tubbs  Pediatric Neurosurgery, Children’s Hospital, Birmingham, AL, USA M. Loukas  Department of Anatomy, Medical School Varmia and Mazuria, Olsztyn, Poland

Case report We present a case of a unilateral occurrence of a variant MMA arising directly from the ophthalmic artery in a human adult formalin-fixed cadaveric head. The artery was discovered during dissection in the medical gross anatomy laboratory at St. George’s University School of Medicine in 73-year-old female Caucasian cadaver. The medical records showed no evidence of trauma or any previous surgical procedures of the head and neck. The cause of death was due to acute inferior myocardial infarction. During dissection skull base by the author (H.K.) with the aid of a Seiler Evolution xR6 Surgical Microscope, it was noted that the left MMA arose from the lateral-most portion of the superior orbital fissure. The lesser wing of the sphenoid bone and the anterior clinoid process were

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Fig. 1  Artist’s representation of the skull base with left MMA exposed. a Normal anatomy of the MMA. The anastomotic branch between the anterior MMA and lacrimal artery is depicted. b Variant

MMA as described in the case report. Note that the ipsilateral foramen spinosum is absent

carefully drilled to expose the superior orbital fissure (Fig.  2). The MMA was seen originating from the lateral portion of the orbit, and a stepwise dissection of the ophthalmic artery was performed. The ophthalmic artery originated from the internal carotid artery and coursed anteriorly through the orbit in its usual fashion. The ophthalmic artery branched into medial and lateral arteries. The medial branch continued toward the eye; the lateral branch recurred posteriorly before looping anteriorly, coursing through the lateral-most portion of the superior orbital fissure. This variant artery gave origin to the MMA (Fig. 2). The diameter of the MMA at lateral middle cranial fossa was measured as 1.5 mm. The lacrimal artery branched from the first, or anterior loop, of the variant MMA. After tracing the origin of the MMA, the dura was reflected along the middle cranial fossa. It was noted that the ipsilateral foramen spinosum was absent. The foramen spinosum was present on the contralateral side of the head, with the MMA running through it in its usual fashion.

just lateral to the superior orbital fissure, in a dried adult human skull. Royle and Motson [12] reported a case of bilateral absence of the foramen spinosum in a dry adult human male skull. The grooves of the middle meningeal arteries in this case arose from the lateral limits of the superior orbital fissures bilaterally. Lastly, Gabriele and Bell [4] reported three cases of an anomalous meningeal artery originating from the ophthalmic artery on arteriography. Unfortunately, in the aforementioned studies, it was not specified whether the variant MMA arose directly from the ophthalmic artery or branched from the lacrimal artery. However, our study showed the variant MMA arose directly from the ophthalmic artery, and the lacrimal artery branched directly from the variant MMA (Fig. 2b). The exact incidence of the variant MMA arising from the ophthalmic artery is difficult to determine. A prevalence of 0.5 % has been reported previously [11]. McLennan et al. [8] examined 108 dried human skulls and noted that one (0.9 %) specimen had bilateral absence of the foramen spinosum and one (0.9 %) had unilateral absence of the foramen spinosum. Nikolova et al. [10] examined 959 dry adult human skull-sides grouped into three cranial series––contemporary male, medieval male, and medieval female. Complete absence of the foramen spinosum was reported in 5 (0.5 %) of the 959 total skull-sides. None of the 400 contemporary male skull-sides had small or absent foramen spinosums; 1 (0.4 %) of the 279 medieval male skull-sides had an absent foramen spinosum; 4 (1.4 %) of the 280 medieval female skull-sides had absent foramen

Discussion An MMA arising directly from the ophthalmic artery is a rare arterial variation that has seldomly been described in the English literature [1, 4, 6, 10, 12]. Curnow [1] reported a variant MMA arising from the ophthalmic artery in 1873. Low [6] later described bilateral MMA grooves entering the middle cranial fossa from the foramen meningo-orbitale,

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Fig. 2  Superolateral view of the a left middle and anterior fossa skull base and b left orbit. a The lesser wing of the sphenoid and the anterior clinoid process have been removed. The roof of the orbit is exposed, and the optic nerve is retracted medially. The ophthalmic artery originates from the internal carotid and courses anteriorly through the orbit in the usual fashion. The ophthalmic artery then gives a serpentine branch laterally, which courses through the lateralmost portion of the superior orbital fissure (roof removed). The variant origin of the MMA branches to anterior and posterior portions. The foramen spinosum was absent on the left. b The roof of the orbit, lesser wing of the sphenoid, and anterior clinoid process have been removed. The superior rectus muscle is retracted anteriorly; the optic nerve is retracted medially to expose the underlying vasculature. The ophthalmic artery branches into medial and lateral arteries. The medial portion continues toward the eye; the lateral branch recurs posteriorly before looping anteriorly, giving origin to the MMA. The lacrimal artery branches from the first, or anterior loop, of the variant MMA. Top-left insets: superior views of a dry skull base. The red boxes represent the anatomic location of the respective figures. Ant. Loop anterior loop, CN III oculomotor nerve, CN VI abducens nerve, Frontal N frontal nerve, Int. Car. A internal carotid artery, Lacrimal A. lacrimal artery, Mid. Men. A. middle meningeal artery, Opth. A. ophthalmic Artery, Optic N. optic nerve, Post. Loop posterior loop, Sup. Rectus M. superior rectus muscle, V1 ophthalmic division of trigeminal nerve, V2 maxillary division of trigeminal nerve, V3 mandibular division of trigeminal nerve

spinosums; and 1 (0.4 %) had a small foramen spinosum. In all of the cases, the middle meningeal groove originated from the lateral edge of the superior orbital fissure. Embryologically, the MMA is derived from the stapedial artery, which branches from the internal carotid artery [2, 3, 10]. When the stapedial artery is fully developed, it has three branches: the supraorbital, infraorbital, and mandibular. In the 15-mm embryo, the trunk of the stapedial artery atrophies and simultaneously transmits its branches to the internal maxillary artery [2, 3, 10]. Thus, the branches of the stapedial artery are ultimately transferred from the internal carotid system to the external carotid system (Fig. 3). The intracranial part of the MMA develops in a different manner from than its extracranial counterpart. At the 20 mm stage of development, the supraorbital artery branches to form the MMA [3]. The supraorbital artery continues to the orbit [3]. With the exception of the arteries directly supplying the eyeball, the arteries of the orbit are also derived from the superior branch of the embryonic stapedial artery. At the 20 mm stage of development, the stem of the ophthalmic artery annexes the superior branch of the stapedial artery (the ramus superior) near the optic nerve [2]. Subsequently, the connection between the intracranial and intraorbital portions of the ramus superior involutes. The ramus superior persists into adulthood as the intracranial part of the MMA [2, 3, 10]. The ophthalmic origin of the MMA involves two separate processes: (1) failure of the proximal intraorbital and retroorbital branches to involute so that the intracranial segments of the MMA remain connected with the intraorbital stapedial branches, and (2) defective involution of the maxillofacial division (ramus inferior) of the stapedial artery so that the extracranial segment of the MMA is never formed [2]. As a result, no connection forms between the maxillary artery and the intracranial segment of the MMA. A variant MMA arising directly from the ophthalmic artery has direct surgical significance. The MMA is an important anatomic landmark to the neurosurgeon when accessing the middle cranial fossa via a temporal craniotomy. It can be followed proximally to help to identify the foramen spinosum and relative position of the greater petrosal nerve and foramen ovale. Additionally, the MMA is usually sacrificed to better expose the middle cranial fossa during a temporal craniotomy. Although there have been no reports to date, a variant MMA arising from the ophthalmic artery may prove difficult to identify and ligate during a temporal craniotomy [10]. Surgical complications may include hemorrhage if the variant arterial anatomy is not identified. Furthermore, because the MMA is such an important anatomic landmark for middle cranial fossa exposure during a temporal craniotomy, great care must be

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Fig. 3  Artist’s diagram depicting the embryologic development of the middle meningeal and ophthalmic arteries. The top line represents normal arterial embryologic development. The bottom line represents the embryologic development of a variant MMA originating from the ophthalmic artery, as described in the case report. Ext. Carotid external carotid, Int. Carotid internal carotid

taken when elevating the dura when a variant MMA exists. The greater petrosal nerve may be avulsed when elevating the dura containing a variant MMA if appropriate landmarks are not first identified. Lastly, it may be possible for variant middle meningeal arteries to contribute to pathology. Maiuri et al. [7] described three cases in which an anomalous MMA originating from the ophthalmic artery was supplying intracranial meningiomas. Conflict of interest The authors declare that they have no conflict of interest.

References 1. Curnow J (1873) Two instances of irregular ophthalmic and middle meningeal arteries. J Anat Physiol 8:155–156 2. Diamond MK (1991) Homologies of the meningeal-orbital arteries of humans: a reappraisal. J Anat 178:223–241 3. Dilenge D, Ascherl GF (1980) Variations of the ophthalmic and middle meningeal arteries: relation to the embryonic stapedial artery. Am J Neuroradiol 1:45–54

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4. Gabriele OF, Bell D (1967) Ophthalmic origin of the middle meningeal artery. Radiology 89:841–844 5. Lasjaunias PL, Berenstein A, Ter Brugge KG (2001) Surgical neuroangiography, vol 2. Springer, Heidelberg 6. Low FN (1946) An anomalous middle meningeal artery. Anat Rec 95:347–351 7. Maiuri F, Donzelli R, De Divitiis O, Fusco M, Briganti F (1998) Anomalous meningeal branches of the ophthalmic artery feeding meningiomas of the brain convexity. Surg Radiol Anat 20:279–284 8. McLennan JE, Rosenbaum AE, Haughton VM (1974) Internal carotid origins of the middle meningeal artery. The ophthalmicmiddle meningeal and stapedial-middle meningeal arteries. Neuroradiology 7:265–275 9. Moret J, Lasjaunias P, Theron J, Merland IJ (1977) The middle meningeal artery. Its contribution to the vascularization of the orbit. J Neuroradiol 4:225–248 10. Nikolova SY, Toneva DH, Yordanov YA, Lazarov NE (2012) Absence of foramen spinosum and abnormal middle meningeal artery in cranial series. Anthropol Anz 69:351–366 11. Plas B, Bonneville F, Dupuy M, Sol JC, Chaynes P (2013) Bilateral ophthalmic origin of the middle meningeal artery. Neurochirurgie 59:183–186 12. Royle G, Motson R (1973) An anomalous origin of the middle meningeal artery. J Neurol Neurosurg Psychiatr 36:874–876

Variant middle meningeal artery origin from the ophthalmic artery: a case report.

We present a rare case of a variant middle meningeal artery (MMA) originating from the ophthalmic artery. During cadaveric dissection of the cranial b...
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